REFiuNT
No. 33 from Animal Bchariour 32, 2 May 19S4
Aniin. Behav., 1Q84, 32, 52O-527
REDUCTION OF INBREEDING IN A NATURAL HERD OF hORSES
By P. DUNCAN,* C. FEH’, J. C. GLEIZE*, P. MALKAS* & A. M. SCOTTt
:kStatioii Biologique dL’ Ia Tour dii Valat, Le Santhuc, F- 13200 ArIes, France
and
tEquine Research Station, Snailwell Road, New,narkct, Si/foIk, U.K.
Abstract. A genetically-isolated herd of 14 Camargue horses left unmanaged for 6 years produced 58
living foals and developed a social system similar to that of wild horses. Paternity of the foals was
determined by blood-typing, inbreeding coefficients were calculated and were lower than expected on
the hypothesis that mating was random with respect to relatedness. The horses showed reduced levels
of sexual behaviour with members of their entourage as juveniles—mother, herd stallion and maternal
siblings.
Inbreeding is used in artificial selection of
domestic animals in order to lix desired heritable
traits rapidly (Lasley 1972). In the Quartcrhorses
of the King Ranch, for instance, the average
inbreeding Coefficient is 0.049 (Evans et al.
1977).
Close inbreeding, however,’ is known to have
deleterious effects on vigour and fecundity in
many species (see Clutton-Brock & Harvey 1976;
Greenwood 1980) including horses (Bournan &
Bos 1979). Indeed it has been argued that one of
the main functions of juvenile dispersal is the
achievement of outcrossing in mammals and
birds (Greenwood 1980; Dobson 1982).
Feral horses and plains and mountain zebra
live in small closed-membership bands (Klingel
1975). The stallions practise mate-defence poly
gyny and the adults may remain together for
several years. The young born into these bands
are therefore surrounded by close kin (parents
and siblings); generally both sexes transfer out of
their natal band at puberty (Klingel 1975; Penz
horn 1979). It has been argued that the function
of this dispersal is to avoid inbreeding (Feist &
McCullough 1976). In fact there are other
plausible explanations for such transfers: young
males could disperse to avoid reproductive com
petition with their fathers, and individuals of
both sexes might leave to avoid feeding competi
tion with adult group members.
Such hypotheses, which are not mutually
exclusive, are difficult to test by observing stable
social systems. Because young horses generally
move away at puberty, only exceptionally will
close kin have the opportunity to mate; similarly
competition between adults and post-pubertal
young will not often be observed.
We have been fortunate in being able to ob
serve an unstable system in which a domestic
herd of horses developed a feral-type social
system under close surveillance. Kinship was
known, and the herd contained three different
blood-lines, so each horse was exposed to both
close kin and unrelated individuals.
In this paper we test the hypothesis that the
horses avoided close kin in their sexual and social
behaviour.
Materials and Methods
The Horses
The horses were all of the Camargue breed,
which has been established in the Rhône Delta
for hundreds, perhaps thousands of years
(Berriot 1969). While there is no evidence that
these horses have ever lived as wild or feral
animals, they have been managed in large herds
on extensive pastures, with little care until recent
years. Mortality rates of the order of 15 per
year, though exceptional, still occur (personal
observation) and it can be assumed that selective
pressures for behavioural and morphological
characters adapted to the animals’ environment
have been significant in historical times.
The horses are small (135—145 cm at the
shoulder) and reach adult weight (430 kg) at
about 7 years of age (personal observation). They
are hardy and for the period of this study were
given no supplementary fodder or veterinary
treatment.
The herd used for this study has existed on the
Tour du Valat estate in the eastern Camargue at
least since the l930s. No females were ever added
to it. An adult stallion was run with the herd for
breeding each year from April to about Septem
ber, until 1973.
The study herd of 14 animals consisted initially
of a 5-year-old stallion, six mares aged 4—19
years, three 2-year-olds (two males and one
520
DUNCAN liT AL: REDUCTION OF INI3REED1NG IN HORSES
teinale) and four yearlings (two males, two
leniales). Each was serially referenced by a letter—
imuher combination, e.g. Dl, where the letter
idn lied the year of birth (D 1969). They were
released into an area of 300 ha, later increased
to 335 ha, in December 1973 and were left withnut manneement until September 1979.
I )uring the iirst 3 years (1974—1976) the herd’s
social structure was loose arid typical of the
domestic herds (Wells & von Goldschmidt
Rothschild 1979). There was a clear linear domi
nance hierarchy with few reversals between
horses aged over 2 years. Spatial relations were
not rigid, but ‘matriarchal families’ were clearly
distim’uishable, for male and female olfsprinn
generally maintained close relations with their
mothers until their third year. The sex-ratio of
breeding animals was female biased, rising from
33 of males to 47 of males, The nine postpubertal males (over 18 months) all mated during
this period.
Over the next 2 years (J977—l97i), the number
of potential breeders increased to 44 (sex-ratio =
males) and the social structure became
45
more complex, with the appearance of seven
closed—membership bands whose composition
and interactions resembled closely those of the
non—territorial zebra and mustang populations
which have so far been studied.
Foals were born in each month from Novem
ber to August, but not in the other months, so for
this analysis foals born in November and
December were grouped with those of the
following spring. Sixty-two foals were born
during the five years 1975—1979, of which four
died at birth. The numbers of horses present at
the beginning of each foaling season and the
numbers of foals born are shown in Table I.
‘
Field Observations and their Analysis
From April 1974 the herd was visited on at
least 20 days per month for a variety of studies
Table 1. The Numbers of Horses Present at the Beginning
of each I’oaling Season (November), and the Numbers of
Foals which Survived Long Enough to Furnish Blood
Samples
Year
Horses
Foals
1974
1975
1976
1977
14
20
26
6
7
9
34
()
197N
43
13
1979
56
20
(social behaviour, time-budgeting, use of habitat,
etc.). During these visits, which were of variable
frequency and duration, records were made of
the nearest neighbour of each horse at intervals
of at least half an hour. The data for 1979 are
used in this paer: these were collected on a tape
recorder in the held, then grouped by season and
analysed using single linkage cluster analysis
(Morgan et al. 1976). There were always seven
reasonably well-defIned clusters and for the
annual summary, which allowed us to establish
the composition of the social groups, we con
structed a matrix of the number of seasons (out
of live) in which each horse was observed in the
same cluster as each other one (sec Wells & von
Goldschmidt-Rothschild 1979).
A mating was said to occur when a horse, with
penis extended, mounted a female. Matings were
recorded throughout the study, both during
systematic observations and on an ad libiturn
basis whenever they were seen.
Genetic Relationships
For the period bel’ore the study (1948—1973) a
herd log was maintained by the farm manager
(F. Rcnsch, R. Lambert personal communi
cation). The mother of each foal was recorded, as
was the presumed fathcr, the stallion present in
the herd 11 months before the foal was born. Only
a single stallion was present at any one time.
For the study period the father was determined
by the paternity exclusion method. A male was
considered a potential sire from the time it was
18 months old and it was assumed that the foals
were sired by males belonging to the study herd
only, there being no evidence to the contrary.
The blood of each horse was sampled in
September 1979 and the blood-type determined
by standard techniques (Scott 1978). Twenty
einht loci were studied.
For nine foals it was not possible to exclude all
but one stallion. In these cases the likelihood
method was used: if at a given locus the foal in
question has the genotype PQ and the mother
QQ, then potential fathers with the genotype PP
are deemed to be twice as likely to have sired the
foal as potential fathers with heterozygous geno
types of the type PQ (Edwards 1972; Foltz and
Hoogland 1981). Such exclusions were backed
up by held data on matings.
The relatedness of each pair of horses (e.g. 18,
K8), measured as the Additive Relationship (a),
was calculated as described by Evans et al.
(1977):
a18
JC8
-
(a xCl + aIs
ni)
ANIMAL
BEHAVIOUR,
where K8 is the younger horse and Ci, DI its
parents.
Thus if 18, K8 are full siblings then
a18<C1= (Cl is mother of 18)
ajg Dl -4 (Dl is father of 18)
4
a18 x X8
The Inbreeding Coefficient (f) of each horse
(e.g. K8) was calculated as: fI8 -4(aci x Dl).
Expected Levels of Inbreeding
In order to test the hypothesis that the horses
avoided breeding with close kin, we required an
estimate of the probability of a conception bet
ween each female—male pair.
The post-pubertal mares conceived annually
with few exceptions (see below); the stallions on
the other hand, differed greatly in reproductive
success (0—6 foals per year). Reproductive success
was closely correlated with age (see below), and
varied from year to yçar. We therefore weighted
each potential sireedch year by the proportion
of foals he sired in that year,to obtain the proba
bility that he mated with a given mare. As an
example, the expected numbers of fitther—
daughter conceptions (Nx
)) were calculated by
1
Nexp
(in •pj)
(1)
where
in -the number of conceiving daughters of the
ith stallion;
p •the proportion of foals of that year sired
by the ith stallion;
a the number of potential sires (over 18
months).
The expected level of inbreeding (J) for each
foal was calculated by
fexp
(f .p)
(2)
32,
2
522
where JHthe Inbreeding Coeflhcient of the foal
had its mother been impregnated by the ith
stallion.
Results
Determination of Paternity
As a IIrst step the blood types of the horses
sired before the study began were examined in
the light of their genetic relationships deduced
from the herd log. All but one were consistent
with the presumed relationships; the erroneous
one was corrected.
For the 58 surviving foals sired during the
study, all except one potenhal sire could be ex
cluded in 49 cases (85 ). The father of the re
maining nine foals was taken as the most prob
able sire on the basis of a likelihood anal sis
(Table Ii). in each case (except N7) this was the
only one of the possible fathers which had been
seen to mate the mother one gestation length
earlier (11 months). In the case of N7, there was
no record of her mother having been mated by
either of the possible fathers in the previous year,
1978, but the genetically niore likely (Hi) had
been seen in a pre-copulation di;nlay witi’ her in
197$ and had mated her carlie in the study. The
other possible sire, 1-14, had never been observed
to mate this mare: Hi was therefore assumed to
he the father. The parents of each horse are given
in the Appencix.
Twenty-one mares bred successfully, usually
producing a foal each year after puberty (mean
+sD0.954- 0.21 foals per year). Of 14 p0tential sires, six had no offspring (mean + SD
1.49 -2.04 foals). The success of the eight sires
varied considerably, and was closely correlated
with their age (Table III: r---0.98, P<0.0I).
Genetic Relatedness and Inbreeding
The Additive Relationship (a) between each
pair of horses, and the Inbreeding Coefficient (f)
Table II. Foals with More than One Possible Father, with the Results of Likelihood Analyses and Relevant Field Observations
Foal
LI
M7
M8
M9
M13
Nl
N7
NI5
N17
Possible
fathers
G4,
DI,
HI,
(14,
G4,
HI,
HI,
HI,
HI,
H4,
JI
H4
H4
16
1-14
H4
H4
H4
13
Most
Matings observed
probable
father
previous year,
by possible fathers
G4 or H4
Dl
1-Il
G4
G4
HI
Hi
HI
Hi
H4x7
Dl x3
H1x4
G4 x 1
04x2
HI xS
H1x3
HI x8
Remarks
G4 in different band
Ji in different band
H4 in different band
16 in different band
H4 in different band
HI showed pre-mating behaviour
H4 in different band
H4 in different band
Assumed
father
H4
Dl
HI
G4
G4
HI
HI
HI
HI
DUNCAN ET AL: REDUCTION OF INBREEDING IN HORSES
523
of each were calculated as described above. The
resulting matrix (76 x 76) is available on request.
The vaLues of f varied between 0 and 0.344;
their distribution followed a poisson law; the
median value was 0.031.
For each generation of foals the median value
of the observedf was lower than the expected, as
calculated by equation 2 (Fig. I). The dif1rence
was signilicant for the foals sired during the early
years, 1974—1976, with a domestic-type social
structure (Kolmogorov—Smirnov two-sample test
K- 11, N=25, P 0.025) as well as in the
later years, 1977 and 197$, with a feral-type social
structure (1977: K]) 7, N 13, P0.05; 197$:
Al) = 9, N =20, P <0.05). Quantitatively, the re
duction in the median level of inbreeding was
considerable, the observed value never exceeding
half of the expected.
Origin of the Reduction in Inbreeding
The reduction in the level of inbreeding in the
herd could be accounted for if there had been a
general tendency among the females to mate with
the least-related males.
The average Additive Relationship of each sire
with all the reproductive mares, weighted b’: the
number of foals they produced is given in lable
111 together with the number of foals ncr sire.
There was a nositivc, though non—signilicant,
correlation between the two variables (r
5 0.557,
N= 8), so the origin of the reduction in con
sanguinity was sought at the level of individual
male—female relationships, the most consan
guineous being mother—son, father—daughter and
sibling—sibling.
Mother—son (M—S) pairings. The matings ob
served are summarized in Table IV. None of the
stallions was observed to mate with its mother;
the most successful, G4, mated with every mare
except his mother. The four oldest stallions (1)4
to H4) were involved in the great majority of
matings: avoidance of M—S pairings is clearly
shown by these horses with respect to the eight
oldest mares born before the study began (9 to
H2). The only empty cells in this partial matrix
are M—S pairs (G4—9, H I—El, 114—9; the mother
of Dl was not in the herd). The number of
matings per pair is signilicantly lower in M—S
pairs (X= 0, N = 3) than in other pairs (X= 11.8
matings; t= 14.4, P< 0.001; comparison of the
means of small samples, Ion transformation).
No foals were born to M—S pairs, though only
2.51 were expected (equation 1 all years).
Mother—son pairings wcr therefore avoided.
Father—daughter (F—D) pairings. Matings were
observed between similar proportions of F—D
pairs (0.45, N= 11, sec Table IV) and other pairs
(0.50, N= 157: x=°•
0 qf I, P>0.5). Two
foals resulted from F—D matinL’s (G4—J3; G4—
1(5), compared with an expected number of 3.14
(equation I, all years). There was, therefore, no
evidence for any reduction of sexual activity
between such pairs.
The 13 young females, 11 to L3, were all born
in the herd of which Dl was the dominant
stallion. Dl nutted less with these mares (median
0 per heat, W = 13; Table IV) than with the
older mares which had not been born into his
herd (median 2.25 per heat, N 8; P=0.005,
median test with Fisher’s exact probability test).
1)1 sired foals with each of the older mares, but
0.12
0.10
-
-
EKpecled
C
Table 111. Age, Total Number of Offsp-ing and Relatedness
to Mares* of the Effective Sires During tile Years 1974—
1978
0
w
0
0
0’
C
Sires
Dl
G4
HI
1-14
13
14
15
16
Age
(years in 1979)
Offspring
10
7
6
6
18
19
7
4
5
4
5
5
3
2
1
5
Relatedness
to mares
0.103
0.242
0.163
0.166
0T0
0.131
0.145
0.12$
0.08
0.06
0
.0
C
0.04
002
Observed
-
-
C—
I
-t
--
76
77
78
Ye r
.
*The average relatedness of each sire to the mares,
weighted by the number of foa!s they produced, is 1vcn.
Fig. 1. Fxected and observed values of the Inbreeding
CoeffIcient of Ibals sired in the years 1974—i 978.
ANIMAL
32,
BEHAVIOUR,
524
2
Table IV. Matings Observed Between Breeding Mares and the Stallions of the Study
Herd, 1974—1979
Stallions
—
Mares
9
5
7
Cl
1)2
11
G3
1-12
11
12
17
18
J3
J4
J5
J6
K2
K5
K7,
LI
L3
1)1
G4
14
13
15
10
9
16
13
25
3
4
it
It
1
*
t
+
t
t
13
38
3
3
18
23
12
24
2
4t
13
It
6
3
6
2
3t
HI
6
2
33
9
12
*
6
7*
11
3*
4
10
1
1
7t
‘
2
2
§
H4
13
14
15
*
1
16
*
1
5
4
2
14
6
6*
6
2*
*
8
§
§
§
5
3
*
*
28
7
6*
2*
t
2
8
6
11
2
11
2
1
1
it
7
3
I
1
t
§
4
+
11
5
3
1
§
Number
of
heats
6
6
6
6
6
6
6
6
5
4
3
3
3
3
3
2
3
2
2
2
2
‘Mother—son pars.
tFailr__daugter pairs.
SiNings which at some stage were part of the same matriarchal family.
Othcr siblings.
ith none of the younger mares (P<0.005,
Fisher’s exact probability test).
There was therefore no evidence for avoidance
of father—daughter matings, but there was a re
duction of sexual activity between fillies and the
stallion of their natal band.
Sibling pairings. Mating was observed in a
similar proportion of sibling (half and full) pairs
as in non-sibling pairs (0.54, 0.51; N=26, 142;
see Table lv). Seven foals were born to siblings,
compared with 9.32 expected (equation 1, all
years). There was, therefore. no evidence for
avoidance of sexual relations between siblings in
general.
Nine of the sibling pairs had experience of
their relationship as they had been contemporary
members of the same matriarchal family. The
frequency of matings between these siblings
(median = 0, N= 9) was lower than between
other siblings (median =2 per heat; N= 17;
P 0.05, median test with Fisher’s exact proba
bility). In one of the rare cases of a known—
sibling mating the observer reported that the
female made considerable efforts to escape. No
foals were born to known sibling pairs, but only
1.6 were expected; see equation 1.
There was therefore some evidence for reduced
sexual activity between siblings which had asso
ciated simultaneously with their mother, but
none between siblings in general.
Social Structnrc and Genetic Rclatcdness
The original herd divided into seven bands in
the years 1977—1978. These bands contained one
or two stallions and two to nine reproductive
mares (Fi. 2). No further transfers of adults
have occurred between these bands (up to
December 1982).
The average Additive Relationship of each
stallion with tilC mares of its own, and of the
other bands is given in Table 1V. Most of the
stallions were less related to maiDs of their own
bands than to the mares in other bands, and the
ditYercncewas signilicant (N 9: T 4; P<0.05;
Wilcoxon matched-pairs, signed-ranks test).
There was therefore evidence that, when forming
permanent social bonds, the horses preferred un
related or distantly—related individuals to close
kin.
None of the pairs mother—son, filly—stallion—of—
natal-band or contemporary maternal siblings
occurred among the adult horses of these bands
525
DUNCAN ET AL.: REDUCTION OF INBREEDfl1G IN HORSES
i:E 1 ± 11
orse
Band
DI
Cl
HI
7
Dl
Dli
G3
HI
H4 J2
El L3
13 JB
12
13
14
14
17
j3
Li
H4
JI
IL
K4
LG
E
C4 5 ii J4 K2 K7
15 H2 is 5 (5
04
Fig. 2. Single linkage cluster analysis of the proximity relations of the post-pubertal
horses in 1979.
(see Fig. 1 and Table V). There were, however,
one pair of non—contemporary maternal siblings
(16—L6), one of paternal siblings (Jl—K4) and
two father—daughter pairs (G4—K5, G4—K7).
Discussion
The application of the blood-typing method for
the determinatn of paternity was aided in this
study by the fact thatwe had a small mriber of
stallions which were rasonabiy polymorphic at
the 28 loci we examined.
This method provided unequivocal results for
the great majority of foals (85 j; paternity of
the remaining foals was determined by likehhood
analysis, the conclusions of which were consistent
with feld observations of sexual behaviour.
As in many species, reproductive success
varied less between females (0—I foal per year)
than between males (0—6 foals sired per year).
The success of a male over the 5 years was closely
related to his age, which in turn was correlated
with his dominance status in the early years
(r=0.9c, calculated from data in Wells & von
Goldschmidt-Rothschild 1979).
Under these semi-natural conditions the levels
of inbreeding remained low (median inbreeding
coefficient <0.04 each year). The expected level,
calculated by weighting each stallion according
to his reproductive success, was signilIcantly
higher, both during the early years and after the
division of the herd.
This reduction of inbreeding did not result
from any general tendency of the mares to mate
with less-related stallions for there was a positive,
though non-significant, correlation between the
stallions’ reproductive success and their average
relatedness to the mares.
The most consanguineous offspring result
from parent—offspring and sibling matings. Both
occurred and resulted in offspring in this herd.
The horses did not, therefore, recognize and
avoid all close kin. There was, however, an
avoidance of mother—son pairings. There were
also reduced levels of sexual behaviour between
lillies and the stallion of their natal band, who
would normally be their father, and between
maternal siblings which had been contemporary
members of their mother’s matriarchal family.
These horses ther’lore showed reduced levels of
sexual activity with the members of their im
mediate social entourage when juvenile, not with
close kin per Se. These results do not provide
evidence for genetically-based recognition of
close kin such as has been lound in some species
(e.g. pigtail macaques, Wu et a!. 1980), but they
do imply that the mechanisms which led to the
reduction of inbreeding were based on experi
ence. This kind of sexual imnrinting has been
found in a number of other mammals (e.g.
Hoogiand 1982) and in birds (e.g. Bateson 1978)
and is considered to be a primary mechanism of
incest avoidance in animal societies (Harvey
et al. 1980).
The development of long-lasting social bonds
between adult males and females in the year
1977—1978 followed the pattern of sexual rela
tionship in the early years. There was no general
avoidance of close kin, but mother—son, lilly—
stall ion-of-natal-band and contemporary materTable V. The Stallions’ Average Additive Relationship
With Mares in Their Own and in Other Baiids
Average additive relationship
Stallions
1
G4
15
1-Il
1-14
13
14
16
JI
median
Own mares
Other mares
0
0.20
0.20
0.27
0.09
0.18
0.07
0.07
0.06
0.14
0.18
0.09
0.15
0.15
0.20
0.12
0.13
0.11
0.20
0.15
ANIMAL
BEHAVIOUR,
nal siblings did not occur in the same bands. As a
consequence most stallions had relativelyunrelated mares in their bands.
These horses showed behaviour patterns which
led to the reduction of inbreeding without the
complex social organization which is found in
wild herds. It is therefore probable that the dis
persal of young horses which, in mature societies,
generally occurs at puberty (e.g. Penzhorn 1979)
is a consequence of the reduced levels of sexual
activity between the young horses and their
immediate entourage.
32,
2
526
Acknowledgments
This study was funded by the Foundation Tour
du Valat and the Equine Research Laboratory of
the Animal Health Trust (A. M. Scott). We are
most grateful to all our colleagues who helped to
collect the behavioural data and to catch the
horses for the blood sampling. Pamela Moncur
and Melanie Barclay carried out the tedious
calculations for the matrix of Additive Relation
ships. The text was considerably improved as a
result of the comments of two anonymous
referees.
Appendix. Parentage of Horses in the Tour du Valat Herd, 1974—1979
Horse
Sex
Mother
Father
9
5
7
Cl
Dl
1)2
II
G2
F
F
F
F
M
F
F
M
Xi
Xl
9
X5’
X7
5
7
X5
X2
X3
X4
X6
X8
X9
X9
X9
(13
(14
F
M
XIO
9
HI
M
El
112
H3
F
F
5
7
X9
X9
XII
Xli
Xli
114
Ii
12
13
14
15
16
17
18
11
J2
J3
J4
J5
.16
J7
Kit
K2
K3
K4
KS
K6t
K7
K8
Lit
M
F
F
M
M
M
M
F
F
M
F
F
F
F
F
M
M
F
M
F
F
M
F
M
F
9
Cl
D2
7
5
El
(13
9
Cl
7
D2
El
5
G3
9
Cl
7
1)2
El
H2
5
(13
11
Cl
7
Xli
X12
XII
X12
X12
X12
X12
Dl
DI
DI
Dl
(14
Dl
Dl
DI
(14
(14
Dl
(14
Dl
G4
(14
G4
Dl
1-14
Year of
birth
1955
1961
1964
1968
1969
1969
1970
1972
(1976)
1976
1976
973
1973
1973
(1075)
1975
1974
1974
1974
1974
1974
1974
1974
1974
1975
1975
1975
1975
1975
1975
1975
1076
1976
1976
1976
1976
1976
976
1976
1977
Horse
Sex
Mother
L2
L3
L4
L5
M
F
M
M
F
M
M
F
F
M
D2
El
12
5
(13
H2
9
[1
18
El
J3
J4
J5
5
17
112
12
G3
J6
K2
CI
1)2
ii
K5
II
J3
18
9
5
K7
J4
J5
17
12
H2
G3
Ll
7
L3
K2
L6
L7
L$
Mi
M2
M3
M4*
M5
M6
M7
MX
M9
M101
Mu
M12t
M13
M14
NI
N2
N3*
N4
N5
N6
N7
N8
N9
Nl0
NIl
Nl2
N13
N14
Nl5
N16
NI7
NIS
N19
F
M
M
F
M
F
M
M
M
M
F
M
F
M
M
F
M
F
M
F
M
M
M
M
F
F
F
M
F
F
Father
H4
Dl
13
11
1-14
1)1
Di
(14
HI
Dl
(14
(14
13
1)1
HI
(14
HI
11
(14
(14
Dl
i-tI
H4
(14
(14
14
(14
HI
(14
13
(14
(14
14
13
15
Hi
14
Hi
16
15
Those horses which were not part of the study herd are indicated by a code name consisting of X+number.
Year of death, where appropriate, is given in parentheses.
Type of mating:
*Fatherdaughter.
tSibiings not from same matriarchal family.
Year of
birth
1977
1977
1977
1977
1977
1977
1977
1978
1978
1976
1978
1978
1978
1978
197$
1978
1978
197$
1978
1978
1)78
197’)
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1079
1979
1979
1979
1979
1979
1979
527
DUNCAN ET AL.: REDUCTION OF INBREEDING IN HORSES
RE FE RE N C ES
Bateson, P. 1978. Sexual imprinting and optimal out
breeding. Nature, Lund., 273, 659—660.
Berriot, C. 1969. I.e cheval de Camargue. D.Vet. thesis,
Ecole Nationale Vétéri naire, Lyon, France.
Bouman, J. G. & Bos, H. 1979. Two symptoms of in
breeding depression in Przewalski horses living in
captivity. In: Genetics (:11(1 Ilcrc’thlary Diseases of
the Prrewalski horse (Ed. by I. Bouman & J. T.
Bouman), pp. 111—117. Rotterdam: Foundation
for the Przewalski Horse.
Clutton-Brock, T. H. & Harvey, P. H. 1976. Evolutionary
rules and primate societies. In: Growing J’oints in
Ethology (Ed. by P. P. G. Bateson & R. A. Hinde),
pp. 195—237. Cambridge: Cambridge University
Press.
Dobson, F. A. 1982. Competition for mates and pre
dominant juvenile male dispersal in manmals.
ilnin,. Behav., 30, 1183—-I 192.
Edwards, A. F. W. 1972. L7kelihood. Cambridge:
Cambridge University Press.
Evans, 3. W., Bortori, A., Hint,, ii. F. & van Vieck, I.. D.
1977. The Horn’. San I rancisco: \V. 11. Freemnn.
Feist, J. D. & Mccullough, 1). R. 1976. iichaviour pat
temns andcommunication in dral horses. Z. 11cr—
psychol., 41, 337--371.
Foltz, D. \V. & HoogIand, 3. I.. 1981. Analysis of the
mating system in the black-tailed prairie dog
(Cvnomys indovicianus) by likelihood of paternity.
J. Mammal., 62, 706—711.
Greenwood, P. J. 1980. Mating systems, philopatry and
dispersal in birds and mammals. Anün. Behav., 28,
1140—1162.
1-farvey. P. H., Baker. M. C., Bateson, P., Bischof, N.,
Emlen. S. ‘1’., 1-lolldobler, B., Kramer, B., Linsen
mair, K. E., Markl, 1-I., Marler. P.. Mcnzel, F. W.,
Mielseuer, C. I)., Milinski, M. & Trillmich, 1’.
1980. Mechanisms of kin-correlated behaviour.
Group report. In: Evolution of Social Behaviour:
hypotheses and LnI,nirical Tests (fEd, by I-I. Markl),
pp. 183—202. Weinheini: Verlag Chemic.
Hoogland, 3. L. 1982. Prairie dogs avoid extreme in
breeding. Science, N. Y., 215, 1639—1641.
Klingcl, H. 1975. Social organisai.ion and reproduction
in equids. J. Reprod. Ten., Suppl., 23, 7—11.
Lasley, J. F’. 1972. Geia’tic. of Livestock Iinprovi’nzcnt.
Englewood Cliffs, New Jersey: l’rcritice Hall.
Morgan, 0. J. T., Simpson, M. 3. A., 1-Lanby, J. P. &
i-lall-Craggc, 3. 1976. Theory and application of
cluster analysis. Beharlour, 56, 1—43.
Penzhorn. B. L. 1979. Social organisation of the Cape
Mountain zebra Equus a. :‘bru in the Mountain
Zebra National Park. lEoec/oe, 22, 115—156.
Scott, A. M. 1978. Immunogenetic analysis as a means of
identi6cation in horses. In: I’roceedin’s oft/ic IVth
Intirnatumal Coi,ç’i’eas on Lquine Infectious Dis—
eases (Ed. by 3. J. llryans & Ii. Gerber), pp. 259—
268. Princeton, New Jersey: Veterinary Publica
tions.
Wells, S. M. & von Goldschmidt-Rothschild, B. 1979.
Social behaviour and relalionships in a herd of
(‘arnarguc horses. Z. Tierpsychol., 4, 363—30.
Wu, H. M.Ff., Holmes, W. 0., Medina, S. R. & Sackett,
0. P. 1980. Kin preference in infant Macaca
nena’strj,,a. Nature, Lond., 285, 225—227.
(Received 10 Mm’ 1982: revived 7 June 1983;
MS. tuimber: 2252)